Ovarian ultrastructure and vitellogenesis in ten species of shallow-water and bathyal sea cucumbers (Echinodermata: Holothuroidea)

Abstract

Comparative ultrastructural features of the ovary and vitellogenesis have been described for six shallow water and four bathyal species of sea cucumbers representing four major holothuroid orders. Ovarian structure is similar in all ten species except for features of the peritoneal cells of the outer layer and the follicular inner epithelial cells surrounding the developing oocytes. The peritoneal cells vary from monociliated squamous or cuboidal cells to large columnar cells. Ultrastructural evidence suggests that these cells might be capable of incorporating materials from the perivisceral coelom. The follicular inner epithelial cells of two deep-sea species resemble podocytes, a feature previously unre-ported in holothuroid ovaries. It is suggested that these cells function to increase nutrient exchange between the genital haemal sinus and the oocyte during vitellogenesis. In all ten species, the oocytes appear to participate in yolk synthesis through the interaction of the Golgi complex and rough endoplasmic reticulum. The similarity in the ultrastructural features of vitellogenesis suggests that the process of yolk synthesis has been highly conserved in holothuroids. Endocytotic activity was detected in seven of ten species but it is uncertain if this is directly related to vitellogenesis. Cilia and intracellular structures resembling striated ciliary rootlets were observed in the oocytes of four of the ten species studied. The significance of this finding is unclear but could indicate that germ cells have a somatic cell origin.

Morphology of the Ovotestis of Synaptula hydriformis (Holothuroidea, Apoda): An Evolutionary Model of Oogenesis and the Origin of Egg Polarity in Echinoderms

“…This study does not address whether somatic cells transform into germ cells, but it does indicate that the oogonia and oocytes of Synaptula hydriformis (like spermatogonia and spermatocytes) are epithelial cells and retain epithelial characteristics, such as intercellular junctions and apical-basal polarity, throughout oogenesis. The occurrence of an apical flagellum, at least into vitellogenic oocytes of S. hydriformis, as shown in this report, and on previtellogenic oocytes of Leptosynapta clarki (Eckelbarger & Young 1992) and Bathyplotes natans (Tyler et al 1994) further support the idea that germ cells are epithelial in holothuroids. The epithelial apical-basal polarity of S. hydriformis gonial cells is retained as the tail-head polarity of the sperms and the animal-vegetal polarity of the eggs, as…”

“…Instead, a synchronized differentiation of gametes in each gonadal tubule is reported to typify holothuroid gametogenesis (Smiley & Cloney 1985; Smiley 1988Smiley , 1990Smiley , 1994Smiley et al 1991). Several species of holothuroids, however, have been shown to exhibit asynchronous differentiation (Eckelbarger & Young 1992).…”

“…Although cohorts of eggs and sperms differentiate as a group, several cohorts of different ages develop simultaneously, as might be expected of a continuously iteroparous species that reproduces on multiple occasions each year. As more species of holothuroids are being examined (Eckelbarger & Young 1992;Sewell & Chia 1994;Tyler et al 1994), synchronous development of all gametes within each gonadal tubule does not appear to be the rule of holothuroid oogenesis, refuting Smiley's claim to the contrary (Smiley 1988(Smiley , 1990(Smiley , 1994. Rather than assuming that all species of any class should have the same re- Amebocytes, also referred to as phagocytes (Hyman 1955), commonly occur throughout the hemal system of most echinoderms (Smiley 1990).…”

“…24, Smiley 1988; figs. 3A, 51, Eckelbarger & Young 1992;Tyler et al 1994). Oocytes of several species of holothuroids, in fact, were previously thought to originate in and remain part of the connective tissue or to migrate from the connective tissue, through the epithelium, into the gonadal lumen, because their linkage to the germinal epithelium was not observed with light microscopy (Clark 1898;Menker 1970;Hansen 1975;Green 1978;Estabrooks 1984).…”

“…Nevertheless, no one except Smiley (1988,1991) has described echinoderm oogonia, or the primordial germ cells from which they arise, as epithelial cells, although crinoid (Holland 1991) and holothuroid (Eckelbarger & Young 1992;Tyler et al 1994) germ cells have been suggested to arise from the somatic epithelial cells of the gonad. This study does not address whether somatic cells transform into germ cells, but it does indicate that the oogonia and oocytes of Synaptula hydriformis (like spermatogonia and spermatocytes) are epithelial cells and retain epithelial characteristics, such as intercellular junctions and apical-basal polarity, throughout oogenesis.…”